Alternative transcription start site selection in Mr-OPY2 controls lifestyle transitions in the fungus Metarhizium robertsii

Proc. Natl. Acad. Sci. U.S.A.

Chen

et al. 2019

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The emergence of new pathogenic fungi has profoundly impacted global biota, but the underlying mechanisms behind host shifts remain largely unknown. The endophytic insect pathogen Metarhizium robertsii evolved from fungi that were plant associates, and entomopathogenicity is a more recently acquired adaptation. Here we report that the broad host-range entomopathogen M. robertsii has 18 genes that are derived via horizontal gene transfer (HGT). The necessity of degrading insect cuticle served as a major selective pressure to retain these genes, as 12 are up-regulated during penetration; 6 were confirmed to have a role in penetration, and their collective actions are indispensable for infection. Two lipid-carrier genes are involved in utilizing epicuticular lipids, and a third (MrNPC2a) facilitates hemocoel colonization. Three proteases degraded the procuticular protein matrix, which facilitated up-regulation of other cuticle-degrading enzymes. The three lipid carriers and one of the proteases are present in all analyzed Metarhizium species and are essential for entomopathogenicity. Acquisition of another protease (MAA_01413) in an ancestor of broad host-range lineages contributed to their host-range expansion, as heterologous expression in the locust specialist Metarhizium acridum enabled it to kill caterpillars. Our work reveals that HGT was a key mechanism in the emergence of entomopathogenicity in Metarhizium from a plant-associated ancestor and in subsequent host-range expansion by some Metarhizium lineages.

Section: Methodsmentioning

confidence: 99%

“…Two thirds (n = 12) of the HGT genes were up-regulated during cuticle penetration ( Fig. 2A), in contrast to only 7% of M. robertsii genes overall (15).…”

Section: Significancementioning

confidence: 99%

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Horizontal gene transfer allowed the emergence of broad host range entomopathogens

Proc. Natl. Acad. Sci. U.S.A.

Chen

et al. 2019

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“…This worldwide distribution is largely attributed to the diverse lifestyles of Metarhizium species, and their tolerance to a broad range of environmental stresses including UV radiation and extreme temperatures [ 11 – 13 ]. Metarhizium has versatile lifestyles: it is a pathogen of arthropods, a saprophyte, and a colonizer of rhizosphere and plant roots [ 14 ]. The genomes of seven Metarhizium species ( Metarhizium robertsii , M .…”

Section: Introductionmentioning

confidence: 99%

Duplication of a Pks gene cluster and subsequent functional diversification facilitate environmental adaptation in Metarhizium species

Zeng

et al. 2018

PLoS Genet

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The ecological importance of the duplication and diversification of gene clusters that synthesize secondary metabolites in fungi remains poorly understood. Here, we demonstrated that the duplication and subsequent diversification of a gene cluster produced two polyketide synthase gene clusters in the cosmopolitan fungal genus Metarhizium. Diversification occurred in the promoter regions and the exon-intron structures of the two Pks paralogs (Pks1 and Pks2). These two Pks genes have distinct expression patterns, with Pks1 highly expressed during conidiation and Pks2 highly expressed during infection. Different upstream signaling pathways were found to regulate the two Pks genes. Pks1 is positively regulated by Hog1-MAPK, Slt2-MAPK and Mr-OPY2, while Pks2 is positively regulated by Fus3-MAPK and negatively regulated by Mr-OPY2. Pks1 and Pks2 have been subjected to positive selection and synthesize different secondary metabolites. PKS1 is involved in synthesis of an anthraquinone derivative, and contributes to conidial pigmentation, which plays an important role in fungal tolerance to UV radiation and extreme temperatures. Disruption of the Pks2 gene delayed formation of infectious structures and increased the time taken to kill insects, indicating that Pks2 contributes to pathogenesis. Thus, the duplication of a Pks gene cluster and its subsequent functional diversification has increased the adaptive flexibility of Metarhizium species.

“…The cosmopolitan fungus Metarhizium robertsii has versatile lifestyles; it is a pathogen of arthropods, a saprophyte and a colonizer of the rhizosphere and plant root (Roberts and St. Leger, 2004;Behie et al, 2012;2017;Guo et al, 2017). A multiyear field trial revealed that the ability of M. robertsii to maintain large populations is determined by its tolerance to abiotic stresses including temperature fluctuation and UV radiation (Fang and St. Leger, 2010;Wang et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Stress‐induced pyruvate accumulation contributes to cross protection in a fungus

Environmental Microbiology

Leger

Fang

2018

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It is commonly observed that microorganisms subjected to a mild stress develop tolerance not only to higher doses of the same stress but also to other stresses - a phenomenon called cross protection. The mechanisms for cross protection have not been fully revealed. Here, we report that heat shock induced cross protection against UV, oxidative and osmotic/salt stress conditions in the cosmopolitan fungus Metarhizium robertsii. Similarly, oxidative and osmotic/salt stresses also induced cross protection against multiple other stresses. We found that oxidative and osmotic/salt stresses produce an accumulation of pyruvate that scavenges stress-induced reactive oxygen species and promotes fungal growth. Thus, stress-induced pyruvate accumulation contributes to cross protection. RNA-seq and qRT-PCR analyses showed that UV, osmotic/salt and oxidative stress conditions decrease the expression level of pyruvate consumption genes in the trichloroacetic acid cycle and fermentation pathways leading to pyruvate accumulation. Our work presents a novel mechanism for cross protection in microorganisms.